Home LiteratureArticle Details
PMID: 6259217 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Antagonism between epidermal growth factor and phorbol ester tumor promoters in human breast cancer cells.

The Journal of clinical investigation ·Vol. 67 ·No. 4 ·1981-04-00 ·Pages 943-51

Osborne CK, Hamilton B, Nover M, Ziegler J

Abstract

It has been suggested that the phorbol ester tumor promoters act via the receptor-effector system for epidermal growth factor (EGF), since they interact with the EGF receptor system and mimic many of the effects of EGF in cultured cells. We have studied the interaction of phorbol esters with the EGF-responsive MCF-7 human breast cancer cell line. Similar to other systems, phorbol esters inhibit EGF binding in MCF-7 cells in a manner paralleling their potency as tumor promoters in mice. The effect is specific for EGF since the membrane binding of insulin is unaffected. Like EGF, the potent phorbol ester 12-O-tetradecanoyl-13-phorbol acetate (TPA) stimulates protein synthesis as indicated by a twofold increase in [(3)H]leucine incorporation into protein after 24 h in TPA. Cell morphology, however, is significantly different with TPA treatment. After 24-48 h in TPA, cells become markedly enlarged with increased cytoplasmic vacuolization and increased membrane microvilli. This is reflected in a fourfold increase in the protein/DNA ratio (control 13.1; TPA 55.9). Furthermore, TPA inhibits cell division in media with or without serum, and prevents growth stimulation by EGF. Low TPA concentrations (1.0 ng/ml) are active, and 10 ng/ml results in maximal inhibition of cell replication. Other phorbol esters inhibit MCF-7 cells relative to their tumor promoting activity in vivo and their ability to inhibit EGF binding in these cells. After 24 h in TPA, incorporation of [(3)H]thymidine into DNA is markedly reduced and the thymidine labeling index falls (33% to 2%) indicating very few S-phase cells. Growth inhibition is reversible by removing TPA from the medium. Similar inhibitory effects are seen with the two other human breast cancer cell lines studied, ZR75-1 and MDA-MB-231. In conclusion, phorbol esters may interact with the EGF receptor domain in MCF-7 human breast cancer cells, but they have distinct effects on cell morphology and growth suggesting alternative pathways of action. The antineoplastic activity of these compounds needs further investigation.

MeSH Terms
Breast Neoplasms/metabolism,pathology Cell Division/drug effects Cell Line DNA, Neoplasm/biosynthesis Epidermal Growth Factor/antagonists & inhibitors,metabolism ErbB Receptors Humans Insulin/metabolism Peptides/antagonists & inhibitors Phorbol Esters/pharmacology Phorbols/pharmacology Receptors, Cell Surface/metabolism
Chemicals
DNA, Neoplasm Insulin Peptides Phorbol Esters Phorbols Receptors, Cell Surface Epidermal Growth Factor ErbB Receptors
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Osborne C K
Hamilton B
Nover M
Ziegler J
References (44)
44 references, click to expand
  1. Inhibition of adipose conversion of 3T3 fibroblasts by tumour promoters.
    Nature. 1977 Sep 15;269(5625):247-9 PMID: 593321
  2. Tumor-promoting phorbol esters inhibit binding of epidermal growth factor to cellular receptors.
    Science. 1978 Oct 20;202(4365):313-5 PMID: 308698
  3. Tumor promoter-mediated inhibition of cell differentiation: suppression of the expression of erythroid functions in murine erythroleukemia cells.
    Proc Natl Acad Sci U S A. 1979 Apr;76(4):1906-10 PMID: 287029
  4. Inhibition of epidermal growth factor binding to surface receptors by tumor promotors.
    Biochem Biophys Res Commun. 1979 Feb 28;86(4):1037-43 PMID: 312103
  5. 125I-labeled human epidermal growth factor. Binding, internalization, and degradation in human fibroblasts.
    J Cell Biol. 1976 Oct;71(1):159-71 PMID: 977646
  6. Induction of terminal differentiation in human promyelocytic leukemia cells by tumor-promoting agents.
    Proc Natl Acad Sci U S A. 1979 Mar;76(3):1293-7 PMID: 286311
  7. Epidermal growth factor, like phorbol esters, induces plasminogen activator in HeLa cells.
    Nature. 1978 Aug 17;274(5672):696-7 PMID: 307695
  8. Tumor promoters: effects on proliferation and differentiation of cells in culture.
    Life Sci. 1978 Nov 13;23(20):1979-88 PMID: 364230
  9. Mechanism of tumor promoter inhibition of cellular binding of epidermal growth factor.
    Proc Natl Acad Sci U S A. 1979 Oct;76(10):5168-72 PMID: 315558
  10. Stimulation of differentiated functions in human melanoma cells by tumor-promoting agents and dimethyl sulfoxide.
    Cancer Res. 1979 Jul;39(7 Pt 1):2618-24 PMID: 445463
  11. Insulin interactions with liver plasma membranes. Independence of binding of the hormone and its degradation.
    J Biol Chem. 1972 Jun 25;247(12):3953-61 PMID: 5033396
  12. A study of the conditions and mechanism of the diphenylamine reaction for the colorimetric estimation of deoxyribonucleic acid.
    Biochem J. 1956 Feb;62(2):315-23 PMID: 13293190
  13. Variants of 3T3 cells lacking mitogenic response to epidermal growth factor.
    Proc Natl Acad Sci U S A. 1977 Sep;74(9):3918-21 PMID: 302945
  14. Effect of tumor promoters on the response of cultured embryonic chick ganglia to nerve growth factor.
    Cancer Res. 1978 Nov;38(11 Pt 1):3886-93 PMID: 698941
  15. The effect of phorbol diesters on chicken embryo fibroblasts.
    Cancer Res. 1977 Sep;37(9):3257-65 PMID: 195722
  16. Ultrastructure of pinealocytes of the cotton rat, Sigmodon hispidus.
    Cell Tissue Res. 1979;204(3):407-16 PMID: 230906
  17. Preparation of iodine-131 labelled human growth hormone of high specific activity.
    Nature. 1962 May 5;194:495-6 PMID: 14450081
  18. Regulation of normal differentiation in mouse and human myeloid leukemic cells by phorbol esters and the mechanism of tumor promotion.
    Proc Natl Acad Sci U S A. 1979 Oct;76(10):5158-62 PMID: 291929
  19. Ornithine decarboxylase induction and DNA synthesis in hamster embryo cell cultures treated with tumor-promoting phorbol diesters.
    Cancer Res. 1977 Nov;37(11):3895-900 PMID: 908030
  20. Binding of epidermal growth factor to primary and permanent cultures of mouse epidermal cells: inhibition by tumor-promoting phorbol esters.
    Cancer Lett. 1979 Jul;7(2-3):71-7 PMID: 314329
  21. Indomethacin inhibition of cell proliferation induced by the phorbolester TPA is reversed by prostaglandin E2 in mouse epidermis in vivo.
    Biochem Biophys Res Commun. 1978 Oct 30;84(4):1103-11 PMID: 728148
  22. Inhibition by prostaglandin synthesis inhibitors of the induction of epidermal ornithine decarboxylase activity, the accumulation of prostaglandins, and tumor promotion caused by 12-O-tetradecanoylphorbol-13-acetate.
    Cancer Res. 1980 Feb;40(2):308-15 PMID: 6243250
  23. Effect of phorbol ester tumor promoters on the expression of melanogenesis in B-16 melanoma cells.
    Cancer Res. 1979 Oct;39(10):3915-9 PMID: 476628
  24. Stimulation of DNA synthesis by tumour promoter and pure mitogenic factors.
    Nature. 1978 Dec 14;276(5689):723-6 PMID: 310518
  25. A human cell line from a pleural effusion derived from a breast carcinoma.
    J Natl Cancer Inst. 1973 Nov;51(5):1409-16 PMID: 4357757
  26. Epidermal growth factor stimulation of human breast cancer cells in culture.
    Cancer Res. 1980 Jul;40(7):2361-6 PMID: 6966967
  27. Tumour promotor induces plasminogen activator.
    Nature. 1976 Jan 22;259(5540):232-3 PMID: 1250353
  28. Induction of differentiation in human promyelocytic leukemia cells by tumor promoters.
    Science. 1979 May 25;204(4395):868-70 PMID: 286421
  29. Human promyelocytic leukemia cells in culture differentiate into macrophage-like cells when treated with a phorbol diester.
    Proc Natl Acad Sci U S A. 1979 Jun;76(6):2779-83 PMID: 288066
  30. Membrane effects of phorbol esters.
    Cancer Res. 1974 Jul;34(7):1731-7 PMID: 4275910
  31. Protein measurement with the Folin phenol reagent.
    J Biol Chem. 1951 Nov;193(1):265-75 PMID: 14907713
  32. Biological and molecular studies of the mitogenic effects of human epidermal growth factor.
    Symp Soc Dev Biol. 1978;(35):13-31 PMID: 306135
  33. Hormone responsive human breast cancer in long-term tissue culture: effect of insulin.
    Proc Natl Acad Sci U S A. 1976 Dec;73(12):4536-40 PMID: 1070004
  34. Inhibition of induced differentiation of C3H/10T 1/2 clone 8 mouse embryo cells by tumor promoters.
    Cancer Res. 1980 Feb;40(2):334-8 PMID: 6153153
  35. Growth of a human mammary tumour cell line in a serum-free medium.
    Nature. 1979 Oct 4;281(5730):388-9 PMID: 481604
  36. Effects of phorbol-12-myristate-13-acetate on the phenotypic program of cultured chondroblasts and fibroblasts.
    Cancer Res. 1978 Aug;38(8):2350-6 PMID: 667832
  37. In vitro determination of thymidine-3H labeling index in human solid tumors.
    Cancer Res. 1974 Jun;34(6):1376-80 PMID: 4363655
  38. Tumor promoters inhibit morphological differentiation in cultured mouse neuroblastoma cells.
    Science. 1978 May 5;200(4341):556-9 PMID: 644318
  39. Tumor promoters induce membrane changes detected by fluorescence polarization.
    Biochem Biophys Res Commun. 1979 Feb 28;86(4):1063-8 PMID: 435310
  40. Effect of a tumour promoter on myogenesis.
    Nature. 1977 Apr 7;266(5602):538-40 PMID: 859620
  41. Epidermal growth factor enhancement of skin tumor induction in mice.
    Experientia. 1976;32(7):913-5 PMID: 954982
  42. Correlation among insulin binding, degradation, and biological activity in human breast cancer cells in long-term tissue culture.
    Cancer Res. 1978 Jan;38(1):94-102 PMID: 22400
  43. Tumor promoters inhibit spontaneous differentiation of Friend erythroleukemia cells in culture.
    Proc Natl Acad Sci U S A. 1977 Jul;74(7):2894-8 PMID: 268640
  44. The tumor promoter 12-O-tetradecanoyl-phorbol-13-acetate enhances the proliferative response of Balb/c-3T3 cells to hormonal growth factors.
    J Cell Physiol. 1979 Sep;100(3):413-24 PMID: 314942
Article Info
Journal
The Journal of clinical investigation
Abbr.
J Clin Invest
ISSN
0021-9738
Published
1981-04-00
Pages
943-51
Language
English
Region
United States
NLM ID
7802877
PMCID
PMC370651
Subset
IM
Grants
NCI NIH HHS · CA 24129 · United States
NICHD NIH HHS · P30 HD 10202 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]